Ancient Tethyan Vicariance and Long-Distance Dispersal Drive Global Diversification and Cryptic Speciation in the Red Seaweed Pterocladiella

Abstract

We investigated the globally distributed red algal genus Pterocladiella, comprising 24 described species, many of which are economically important sources of agar and agarose. We used DNA-based species delimitation approaches, phylogenetic, and historical biogeographical analyses to uncover cryptic diversity and infer the drivers of biogeographic patterns. We delimited 43 species in Pterocladiella, of which 19 are undescribed. Our multigene time-calibrated phylogeny and ancestral area reconstruction indicated that Pterocladiella most likely originated during the Early Cretaceous in the Tethys Sea. Ancient Tethyan vicariance and long-distance dispersal have shaped current distribution patterns. The ancestor of Eastern Pacific species likely arose before the formation of the formidable Eastern Pacific Barrier—a first confirmation using molecular data in red algae. Divergences of Northeast and Southeast Pacific species have been driven by the Central American Seaway barrier, which, paradoxically, served as a dispersal pathway for Atlantic species. Both long- and short-distance dispersal scenarios are supported by genetic relationships within cosmopolitan species based on haplotype analysis. Asymmetrical distributions and the predominance of peripatry and sympatry between sister species suggest the importance of budding speciation in Pterocladiella. Our study highlights the underestimation of global diversity in these crucial components of coastal ecosystems and provides evidence for the complex evolution of current species distributions.

A New Species from the Canary Islands Increases the Diversity of the Red Algal Genus Pterocladiella in the Northeastern Atlantic

“…Phylogenetic analyses using several molecular markers individually and in various combinations have proven to be very useful tools for establishing the differences and similarities among species not detected by morphological studies [ 1 , 2 , 14 , 39 ]. After the recent results presented by Boo et al [ 19 ], Pterocladiella joins a growing list of red algal taxa such as Lithophyllum Philippi [ 40 ], Portieria Zanardini [ 41 ], Polysiphonia Greville [ 42 ], Porolithon Foslie [ 43 ], or Sporolithon Heydrich [ 44 ] for which DNA sequence analyses have resulted in a remarkable increase in species diversity. Pending morphological studies now underway [ 19 ], Pterocladiella currently includes 25 formally described species, to which should be added another 17 genetically differentiated but as yet undescribed species, and two species that must be transferred from Gelidiella .…”

“…Pterocladiella canariensis is also distinct from ‘ Gelidiella calcicola’ Maggs and Guiry [ 21 ] (type locality: Carraroe, County Galway, Ireland), a morphologically similar taxon that has been erroneously identified as P. melanoidea in different localities of the NE Atlantic between Brittany and Portugal [ 22 , 50 ]. According to Boo et al [ 19 ], this taxon belongs to Pterocladiella but it is phylogenetically distantly related to specimens identified as P. melanoidea in the Mediterranean Sea. ‘ Gelidiella calcicola ’ is characterized by plants up to 30 mm in height with terete to flattened erect axes, larger polygonal cortical cells (5–18 µm wide), triangular cystocarp in transverse section, and lacks sterile margin in tetrasporangial sori [ 21 , 22 , 50 , 51 ].…”

“…P. sanctarum (type locality: Îles des Saintes, Guadeloupe, West Indies; also reported from North American and Caribbean Islands) is also a minute species (up to 20 mm height) but differs by erect axes thin and compressed, ending narrower and cylindrical larger square outer cortical cells, and tetrasporangia irregularly arranged or in horizontal rows [ 9 , 54 ]. Finally, ‘Gelidiella feldmannii’ (type locality: Nightingale Island and the Settlement, Tristan da Cunha) is a taxon belonging to Pterocladiella according to molecular evidence [ 19 , 55 ], although to date no new name for this species has been proposed to date. It is also a minute species (up to 15 mm height) but differs by erect axes subcylindrical to flattened, irregularly branched including opposite at right angles or pinnate branches up to two orders [ 55 , 56 ].…”

“…Currently, a total of 25 species with warm-temperate to tropical distributions are accepted in Pterocladiella [ 18 ]. However, recent findings by Boo et al [ 19 ], using DNA-based species delimitation methods, have uncovered a notable cryptic diversity in Pterocladiella , delimiting up to 43 species, of which 19 remain undescribed, including two species hitherto assigned to Gelidiella Feldmann and Hamel.…”

“…Pterocladiella capillacea and P. melanoidea (Schousboe ex Bornet) Santelices and Hommersand have been the only two species of the genus identified in the Northeast Atlantic and the Mediterranean Sea up until now [ 3 , 18 , 20 ]. But according to Boo et al [ 19 ] a third species must be considered since the subtidal Gelidiella calcicola Maggs and Guiry [ 21 ] and the intertidal P. melanoidea sensu Díaz-Tapia and Bárbara [ 22 ] from Atlantic Europe are conspecific and different from P. melanoidea [ 19 ]. Both P. capillacea and P. melanoidea have also been reported from the Canary Islands [ 23 , 24 ].…”